Synchronous Diversification of Sulawesi's Iconic Artiodactyls Driven
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Downloaded from http://rspb.royalsocietypublishing.org/ on April 24, 2018 Synchronous diversification of Sulawesi’s rspb.royalsocietypublishing.org iconic artiodactyls driven by recent geological events Laurent A. F. Frantz1,2,†, Anna Rudzinski3,†, Research Abang Mansyursyah Surya Nugraha4,},†, Allowen Evin5,6,†, James Burton7,8,†, Cite this article: Frantz LAF et al. 2018 Ardern Hulme-Beaman2,6, Anna Linderholm2,9, Ross Barnett2,10, Synchronous diversification of Sulawesi’s iconic Rodrigo Vega11, Evan K. Irving-Pease2, James Haile2,10, Richard Allen2, artiodactyls driven by recent geological events. Kristin Leus12,13, Jill Shephard14,15, Mia Hillyer14,16, Sarah Gillemot14, Proc. R. Soc. B 285: 20172566. 14 17 11 3 http://dx.doi.org/10.1098/rspb.2017.2566 Jeroen van den Hurk , Sharron Ogle , Cristina Atofanei , Mark G. Thomas , Friederike Johansson18, Abdul Haris Mustari19, John Williams20, Kusdiantoro Mohamad21, Chandramaya Siska Damayanti21, Received: 30 November 2017 Ita Djuwita Wiryadik, Dagmar Obbles22, Stephano Mona23,24, Hally Day25, Accepted: 16 March 2018 Muhammad Yasin25, Stefan Meker26, Jimmy A. McGuire27, Ben J. Evans28, Thomas von Rintelen29, Simon Y. W. Ho30, Jeremy B. Searle31, Andrew C. Kitchener32,33, Alastair A. Macdonald7,‡, Darren J. Shaw7,‡, Subject Category: Robert Hall4,‡, Peter Galbusera14,‡ and Greger Larson2,‡ Evolution 1School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK Subject Areas: 2The Palaeogenomics & Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford OX1 3QY, UK genetics, evolution 3Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK 4SE Asia Research Group, Department of Earth Sciences, Royal Holloway University of London, Egham, Keywords: Surrey TW20 0EX, UK biogeography, evolution, geology, Wallacea 5Institut des Sciences de l’Evolution, Universite´ de Montpellier, CNRS, IRD, EPHE, Place Euge`ne Bataillon, 34095 Montpellier, Cedex 05, France 6Department of Archaeology, Classics and Egyptology, University of Liverpool, 12-14 Abercromby Square, Liverpool L69 7WZ, UK Authors for correspondence: 7Royal (Dick) School of Veterinary Studies & The Roslin Institute, University of Edinburgh, Easter Bush Campus, Laurent A. F. Frantz Roslin, Edinburgh EH25 9RG, UK 8IUCN SSC Asian Wild Cattle Specialist Group and Chester Zoo, Cedar House, Caughall Road, Upton by Chester, e-mail: [email protected] Chester CH2 1LH, UK Greger Larson 9Department of Anthropology, Texas A&M University, College Station, TX 77843-4352, USA e-mail: [email protected] 10Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350 Copenhagen K, Denmark 11Ecology Research Group, Section of Life Sciences, School of Human and Life Sciences, Canterbury Christ Church University, North Holmes Road, Canterbury CT1 1QU, Kent, UK 12Copenhagen Zoo, IUCN SSC Conservation Breeding Specialist Group—Europe, Roskildevej 38, Postboks 7, 2000 Frederiksberg, Denmark 13European Association of Zoos and Aquaria, PO Box 20164, 1000 HD Amsterdam, The Netherlands † Contributed equally to this study. 14Centre for Research and Conservation (CRC), Royal Zoological Society of Antwerp, Koningin Astridplein 20-26, }Present address: Pertamina University, Jl. 2018 Antwerp, Belgium 15 Teuku Nyak Arief, Kawasan Simprug, Environment and Conservation Sciences, School of Veterinary and Life Sciences, Murdoch University, Perth, Western Australia 6150, Australia Kebayoran Lama, Jakarta Selatan 12220, 16Molecular Systematics Unit/Terrestrial Zoology, Western Australian Museum, Welshpool, Western Australia, Indonesia. Australia kDeceased. 17Edinburgh Medical School: BMTO, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK 18 ‡Co-supervised the study. Gothenburg Natural History Museum, Box 7283, 402 35 Gothenburg, Sweden 19Department of Forest Resources Conservation and Ecotourism, Faculty of Forestry, Bogor Agricultural University, PO Box 168, Bogor 16001, Indonesia Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9. figshare.c.4040687. & 2018 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Downloaded from http://rspb.royalsocietypublishing.org/ on April 24, 2018 20Davies Research Centre, School of Animal and Veterinary Sciences, Faculty of The geological origins of Wallacea are as complex as its bio- 2 Sciences, University of Adelaide, Roseworthy, Southern Australia 5371, Australia geography. Until recently, Sulawesi had been regarded as the 21 rspb.royalsocietypublishing.org Faculty of Veterinary Medicine, Bogor Agricultural University, Jalan Agatis, product of multiple collisions of continental fragments from IPB Campus, Darmaga, Bogor 16680, Indonesia the Late Cretaceous [6–9]. This assumption has been chal- 22Laboratory of Aquatic Ecology, Evolution and Conservation, KU Leuven, Ch. lenged and a recent reinterpretation suggests instead that the Deberiotstraat 32, 3000 Leuven, Belgium island began to form as the result of continental collisions 23Institut de Syste´matique, E´volution, Biodiversite´, ISYEB - UMR 7205 - CNRS, MNHN, UPMC, EPHE, Ecole Pratique des Hautes Etudes, 16 rue Buffon, CP39, 75005 Paris, during the Cretaceous, which were then followed by Eocene France rifting of the Makassar Strait. This process led to the isolation 24EPHE, PSL Research University, Paris, France of small land areas in western Sulawesi from Sundaland. In 25No affiliation the Early Miocene (approx. 23 Ma), a collision between the 26Department of Zoology, State Museum of Natural History Stuttgart, Rosenstein 1, Sula Spur (a promontory of the Australian continent) and 70191 Stuttgart, Germany north Sulawesi led to uplift and emergence of land [10–12]. Proc. R. Soc. B 27Museum of Vertebrate Zoology and Department of Integrative Biology, University of Later tectonic movements led to the present-day configuration California, Berkeley, CA 94720, USA of islands between Borneo and Australia [13,14]. 28 Department of Biology, McMaster University, Hamilton, Ontario, Canada A previous interpretation, involving the assembly of mul- 29Museum fu¨r Naturkunde - Leibniz Institute for Evolution and Biodiversity Science, tiple terranes by collision, was used to suggest that Sulawesi’s Berlin, Germany 285 30 peculiar species richness resulted from vicariance and amalga- School of Life and Environmental Sciences, University of Sydney, Sydney, New South : 20172566 Wales 2006, Australia mation over long geological time periods [10,15,16]. However, 31Department of Ecology and Evolutionary Biology, Cornell University, Corson Hall, recent molecular-clock analyses suggest that a dispersal, start- Ithaca, NY 14853, USA ing in the Middle Miocene (approx. 15 Ma) from both Sunda 32Department of Natural Sciences, Chambers Street, National Museums Scotland, and Sahul, is a more plausible explanation [17–19]. These con- Edinburgh EH1 1JF, UK clusions suggest a limited potential for animal dispersal to 33Institute of Geography, School of Geosciences, University of Edinburgh, Sulawesi prior to approximately 15 Ma. Rapid tectonic changes, Drummond Street, Edinburgh EH8 9XP, UK coupled with the dramatic sea-level fluctuations over the past LAFF, 0000-0001-8030-3885; AE, 0000-0003-4515-1649; 5 Myr [20] might also have affected land availability and influ- AH-B, 0000-0001-8130-9648; DJS, 0000-0003-2016-1541; enced patterns of species dispersal to Sulawesi, intra-island GL, 0000-0002-4092-0392 species expansion and speciation. The hypothesis of a recent increase in land area [19] can ThehighdegreeofendemismonSulawesihaspreviously be tested by comparing the population histories of multiple been suggested to have vicariant origins, dating back species on the island. Analyses of genetic and morphometric to 40 Ma. Recent studies, however, suggest that much of variability can be used to infer the timing and trajectories of Sulawesi’s fauna assembled over the last 15 Myr. Here, we dispersal, and the geographical and temporal origins of test the hypothesis that more recent uplift of previously expansion. For example, if land area had increased from a submerged portions of land on Sulawesi promoted diversifi- single smaller island, extant species now living on Sulawesi cation and that much of its faunal assemblage is much would all have expanded from the same area. In addition, younger than the island itself. To do so, we combined palaeo- under this assumption, within the same geographical geographical reconstructionswith genetic andmorphometric region their respective diversifications would be expected to datasets derived from Sulawesi’s three largest mammals: the have been roughly simultaneous. babirusa, anoa and Sulawesi warty pig. Our results indicate Here, we focus on three large mammals endemic to that although these species most likely colonized the area Sulawesi: the babirusa (Babyrousa spp.), the Sulawesi warty that is now Sulawesi at different times (14 Ma to 2–3 Ma), pig (SWP, Sus celebensis) and the anoa, a dwarf buffalo (Bubalus they experienced an almost synchronous expansion from spp.). The babirusa is a suid characterized by wrinkled skin the central part of the island. Geological reconstructions and two extraordinary curved upper canine tusks displayed